ARP2/3 complex‐mediated actin dynamics is required for hydrogen peroxide‐induced stomatal closure in Arabidopsis

Abstract

Multiple cellular events like dynamic actin reorganization and hydrogen peroxide (H2O2) production were demonstrated to be involved in abscisic acid (ABA)-induced stomatal closure. However, the relationship between them as well as the underlying mechanisms remains poorly understood. Here, we showed that H2O2 generation is indispensable for ABA induction of actin reorganization in guard cells of Arabidopsis that requires the presence of ARP2/3 complex. H2O2-induced stomatal closure was delayed in the mutants of arpc4 and arpc5, and the rate of actin reorganization was slowed down in arpc4 and arpc5 in response to H2O2, suggesting that ARP2/3-mediated actin nucleation is required for H2O2-induced actin cytoskeleton remodelling. Furthermore, the expression of H2O2 biosynthetic related gene AtrbohD and the accumulation of H2O2 was delayed in response to ABA in arpc4 and arpc5, demonstrating that misregulated actin dynamics affects H2O2 production upon ABA treatment. These results support a possible causal relation between the production of H2O2 and actin dynamics in ABA-mediated guard cell signalling: ABA triggers H2O2 generation that causes the reorganization of the actin cytoskeleton partially mediated by ARP2/3 complex, and ARP2/3 complex-mediated actin dynamics may feedback regulate H2O2 production.

CASEIN KINASE1-LIKE PROTEIN2 Regulates Actin Filament Stability and Stomatal Closure via Phosphorylation of Actin Depolymerizing Factor

“…The essential role of actin dynamics in regulating stomatal closure and opening is well appreciated (Kim et al, 1995;Eun and Lee, 1997;Hwang and Lee, 2001;MacRobbie and Kurup, 2007;Zhao et al, 2011;Jiang et al, 2012;Li et al, 2014), but how actin dynamics are functionally coupled to the underlying cellular processes in guard cells remains poorly understood. For instance, actin dynamics have been implicated in mediating Ca 2+ concentration changes in the cytosol, K + channel activity, and vacuole shape determination (Hwang et al, 1997;Gao et al, 2009;Zhao et al, 2013), but the related molecular mechanisms remain to be established.…”

“…Observation of a single actin filament lifetime, including elongation rate and depolymerizing rate, in living cells has been employed to study actin dynamics in vivo (Smertenko et al, 2010;Henty-Ridilla et al, 2013;Qin et al, 2014;Li et al, 2014;Li et al, 2015). To examine the actin filament dynamics in the guard cells of Col-0 and the ckl2 mutant, we performed time-lapse imaging using spinning disk confocal microscopy to determine single actin filament dynamics ( Figure 4A; Supplemental Movies 1 and 2).…”

“…SCAB1 stabilizes actin filaments, and loss of SCAB1 in plants causes defects in stomatal closure (Zhao et al, 2011). The Arp2/3 complex mediates stomatal closure in response to external stimuli and regulates actin reorganization in guard cells (Jiang et al, 2012;Li et al, 2014). However, how such actin filament reorganization in guard cells is regulated remains an open question.…”

“…The actin cytoskeleton in the guard cells changes from wellorganized cortical filaments in the guard cells of open stomata, to randomly distributed filaments, and then finally reorganizes into highly bundled long cables in the longitudinal direction in the guard cells of closed stomata (Hwang and Lee, 2001;Zhao et al, 2011). This regulatory process involves actin binding proteins such as SCAB1 and the Arp2/3 complex (Zhao et al, 2011;Jiang et al, 2012;Li et al, 2014). SCAB1 stabilizes actin filaments, and loss of SCAB1 in plants causes defects in stomatal closure (Zhao et al, 2011).…”

Capping Protein Modulates Actin Remodeling in Response to Reactive Oxygen Species during Plant Innate Immunity

“…In mammalian cells, ROS regulate actin rearrangements associated with cellular processes such as cell adhesion, migration, wound repair, as well as neurite outgrowth (Chiarugi et al, 2003;Fiaschi et al, 2006;Munnamalai and Suter, 2009;Sakai et al, 2012;Taulet et al, 2012;Xu and Chisholm, 2014). In plant cells, ROS signaling is required for actin remodeling during the self-incompatibility response in pollen tubes and abscisic acid-induced stomatal closure (Wilkins et al, 2011;Li et al, 2014c). In Arabidopsis, flg22-induced stomatal closure also requires NADPH oxidase, RBOHD.…”